Airway nerves and dyspnea associated with inflammatory airway disease

Respiratory Physiology and Neurobiology

Volumn 167, Issue 1, 2009, Pages 36-44

  Undem, Bradley J ^a   Nassenstein, Christina ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Airway inflammation; Asthma; Bronchopulmonary C fibers; Dyspnea; Low threshold mechanosensors; Vagal afferent nerves

Indexed keywords

ACETYLCHOLINE; CORTICOSTEROID; FUROSEMIDE; G PROTEIN COUPLED RECEPTOR; GLIAL CELL DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR; PURINERGIC P2X RECEPTOR; SEROTONIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

AIRFLOW; AIRWAY; AIRWAY OBSTRUCTION; ARTICLE; ASTHMA; AUTONOMIC NERVE; BRAIN STEM; BREATHING; BRONCHUS MUSCLE; DYSPNEA; GENE EXPRESSION; HUMAN; INFLAMMATION; MECHANORECEPTOR; MECHANOTRANSDUCTION; MOLECULAR MECHANICS; MUCUS SECRETION; NERVE CELL; NERVE FIBER C; NERVE FUNCTION; NERVE STIMULATION; NOCICEPTION; NONHUMAN; PARASYMPATHETIC NERVE; PRIORITY JOURNAL; RESPIRATORY NERVE CELL; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; SENSORY NERVE; SMOOTH MUSCLE TONE; SPINAL NERVE; STRETCH RECEPTOR; SYNAPTIC EFFICACY; VAGUS NERVE;

ANIMALS; DYSPNEA; HUMANS; INFLAMMATION; MUSCLE, SMOOTH; NERVE FIBERS, UNMYELINATED; NEURONS, AFFERENT; RESPIRATION DISORDERS; RESPIRATORY SYSTEM; VAGUS NERVE;

EID: 67349141925     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2008.11.012     Document Type: Article

References (123)

1. Anonymous. Long-term effects of budesonide or nedocromil in children with asthma. The Childhood Asthma Management Program Research Group. N. Engl. J. Med. 343 (2000) 1054-1063
2. Ahn M., Beacham D., Westenbroek R.E., Scheuer T., and Catterall W.A. Regulation of Na(v)1.2 channels by brain-derived neurotrophic factor, TrkB, and associated Fyn kinase. J. Neurosci. 27 (2007) 11533-11542
3. Auchincloss J.H., Streeten D.H., Gilbert R., and Peppi D. Dyspnea in patients with hyperbradykininism and excessive venous pooling. Am. J. Med. 81 (1986) 260-266
4. Baker C.V., and Schlosser G. The evolutionary origin of neural crest and placodes. J. Exp. Zool. B: Mol. Dev. Evol. 304 (2005) 269-273
5. Basoglu O.K., Pelleg A., Essilfie-Quaye S., Brindicci C., Barnes P.J., and Kharitonov S.A. Effects of aerosolized adenosine 5′-triphosphate vs adenosine 5′-monophosphate on dyspnea and airway caliber in healthy nonsmokers and patients with asthma. Chest 128 (2005) 1905-1909
6. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., and Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 (2006) 1269-1282
7. Beasley R., Varley J., Robinson C., and Holgate S.T. Cholinergic-mediated bronchoconstriction induced by prostaglandin D2, its initial metabolite 9 alpha,11 beta-PGF2, and PGF2 alpha in asthma. Am. Rev. Respir. Dis. 136 (1987) 1140-1144
8. Bergren D.R. Sensory receptor activation by mediators of defense reflexes in guinea-pig lungs. Respir. Physiol. 108 (1997) 195-204
9. Blum R., Kafitz K.W., and Konnerth A. Neurotrophin-evoked depolarization requires the sodium channel Na(V)1.9. Nature 419 (2002) 687-693
10. Brouns I., Adriaensen D., Burnstock G., and Timmermans J.P. Intraepithelial vagal sensory nerve terminals in rat pulmonary neuroepithelial bodies express P2X(3) receptors. Am. J. Respir. Cell. Mol. Biol. 23 (2000) 52-61
11. Brown R.H., Croisille P., Mudge B., Diemer F.B., Permutt S., and Togias A. Airway narrowing in healthy humans inhaling methacholine without deep inspirations demonstrated by HRCT. Am. J. Respir. Crit. Care Med. 161 (2000) 1256-1263
12. Brown R.H., Herold C., Zerhouni E.A., and Mitzner W. Spontaneous airways constrict during breath holding studied by high-resolution computed tomography. Chest 106 (1994) 920-924
13. Burki N.K., Alam M., and Lee L.Y. The pulmonary effects of intravenous adenosine in asthmatic subjects. Respir. Res. 7 139 (2006) 139
14. Burki N.K., Dale W.J., and Lee L.Y. Intravenous adenosine and dyspnea in humans. J. Appl. Physiol. 98 (2005) 180-185
15. Burki N.K., Sheatt M., and Lee L.Y. Effects of airway anesthesia on dyspnea and ventilatory response to intravenous injection of adenosine in healthy human subjects. Pulm. Pharmacol. Ther. 21 (2008) 208-213
16. Canning B.J. Reflex regulation of airway smooth muscle tone. J. Appl. Physiol. 101 (2006) 971-985
17. Canning B.J., and Fischer A. Neural regulation of airway smooth muscle tone. Respir. Physiol. 125 (2001) 113-127
18. Carr M.J., Kollarik M., Meeker S.N., and Undem B.J. A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals. J. Pharmacol. Exp. Ther. 304 (2003) 1275-1279
19. Carr M.J., and Lee L.Y. Plasticity of peripheral mechanisms of cough. Respir. Physiol. Neurobiol. 152 (2006) 298-311
20. Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., Chao .M.V., and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411 (2001) 957-962
21. Chuaychoo B., Lee M.G., Kollarik M., Pullmann Jr. R., and Undem .B.J. Evidence for both adenosine A1 and A2A receptors activating single vagal sensory C-fibres in guinea pig lungs. J. Physiol. 575 (2006) 481-490
22. Chuaychoo B., Lee M.G., Kollarik M., and Undem B.J. Effect of 5-hydroxytryptamine on vagal C-fiber subtypes in guinea pig lungs. Pulm. Pharmacol. Ther. 18 (2005) 269-276
23. Coleridge H.M., and Coleridge J.C. Impulse activity in afferent vagal C-fibres with endings in the intrapulmonary airways of dogs. Respir. Physiol. 29 (1977) 125-142
24. Coleridge J.C., and Coleridge H.M. Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev. Physiol. Biochem. Pharmacol. 99 1-110 (1984) 1-110
25. Davenport P.W., Lee L.Y., Lee K., Yu L.K., Miller R., and Frazier D.T. Effect of bronchoconstriction on the firing behavior of pulmonary stretch receptors. Respir. Physiol. 46 (1981) 295-307
26. Dinh Q.T., Groneberg D.A., Peiser C., Springer J., Joachim R.A., Arck P.C., Klapp B.F., and Fischer A. Nerve growth factor-induced substance P in capsaicin-insensitive vagal neurons innervating the lower mouse airway. Clin. Exp. Allergy 34 (2004) 1474-1479
27. Diss J.K., Calissano M., Gascoyne D., Djamgoz M.B., and Latchman D.S. Identification and characterization of the promoter region of the Nav1.7 voltage-gated sodium channel gene (SCN9A). Mol. Cell Neurosci. 37 (2008) 537-547
28. Elitt C.M., McIlwrath S.L., Lawson J.J., Malin S.A., Molliver D.C., Cornuet P.K., Koerber H.R., Davis B.M., and Albers K.M. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J. Neurosci. 26 (2006) 8578-8587
29. Empey D.W., Laitinen L.A., Jacobs L., Gold W.M., and Nadel J.A. Mechanisms of bronchial hyperreactivity in normal subjects after upper respiratory tract infection. Am. Rev. Respir. Dis. 113 (1976) 131-139
30. Finnerty J.P., and Holgate S.T. The contribution of histamine release and vagal reflexes, alone and in combination, to exercise-induced asthma. Eur. Respir. J. 6 (1993) 1132-1137
31. Fox A.J., Barnes P.J., and Dray A. Stimulation of guinea-pig tracheal afferent fibres by non-isosmotic and low-chloride stimuli and the effect of frusemide. J. Physiol. 482 (1995) 179-187
32. Fox A.J., Barnes P.J., Urban L., and Dray A. An in vitro study of the properties of single vagal afferents innervating guinea-pig airways. J. Physiol. 469 (1993) 21-35
33. Fuller R.W., Dixon C.M., and Barnes P.J. Bronchoconstrictor response to inhaled capsaicin in humans. J. Appl. Physiol. 58 (1985) 1080-1084
34. Fuller R.W., Dixon C.M., Cuss F.M., and Barnes P.J. Bradykinin-induced bronchoconstriction in humans. Mode of action. Am. Rev. Respir. Dis. 135 (1987) 176-180
35. Grimm D.R., Arias E., Lesser M., Bauman W.A., and Almenoff P.L. Airway hyperresponsiveness to ultrasonically nebulized distilled water in subjects with tetraplegia. J. Appl. Physiol. 86 (1999) 1165-1169
36. Groeben H., and Brown R.H. Ipratropium decreases airway size in dogs by preferential M2 muscarinic receptor blockade in vivo. Anesthesiology 85 (1996) 867-873
37. Groth M., Helbig T., Grau V., Kummer W., and Haberberger R.V. Spinal afferent neurons projecting to the rat lung and pleura express acid sensitive channels. Respir. Res. 7 96 (2006) 96
38. Gu Q., and Lee L.Y. Characterization of acid signaling in rat vagal pulmonary sensory neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 291 (2006) L58-L65
39. Guz A., Noble M.I.M., Eisele J.H., and Trenchard D. Experimental results of vagal block in cardiopulmonary disease. In: Porter R. (Ed). Breathing: Hering-Breuer Centenary Symposium. Churchill, London (1970) 315-329
40. Handforth A., DeGiorgio C.M., Schachter S.C., Uthman B.M., Naritoku D.K., Tecoma E.S., Henry T.R., Collins S.D., Vaughn B.V., Gilmartin R.C., Labar D.R., Morris III G.L., Salinsky M.C., Osorio I., Ristanovic R.K., Labiner D.M., Jones J.C., Murphy J.V., Ney G.C., and Wheless J.W. Vagus nerve stimulation therapy for partial-onset seizures: a randomized active-control trial. Neurology 51 (1998) 48-55
41. Hilborn M.D., Vaillancourt R.R., and Rane S.G. Growth factor receptor tyrosine kinases acutely regulate neuronal sodium channels through the src signaling pathway. J. Neurosci. 18 (1998) 590-600
42. Ho C.Y., Gu Q., Hong J.L., and Lee L.Y. Prostaglandin E(2) enhances chemical and mechanical sensitivities of pulmonary C fibers in the rat. Am. J. Respir. Crit. Care Med. 162 (2000) 528-533
43. Ho C.Y., Gu Q., Lin Y.S., and Lee L.Y. Sensitivity of vagal afferent endings to chemical irritants in the rat lung. Respir. Physiol. 127 (2001) 113-124
44. Hong J.L., Ho C.Y., Kwong K., and Lee L.Y. Activation of pulmonary C fibres by adenosine in anaesthetized rats: role of adenosine A1 receptors. J. Physiol. 508 (1998) 109-118
45. Hong J.L., Kwong K., and Lee L.Y. Stimulation of pulmonary C fibres by lactic acid in rats: contributions of H+ and lactate ions. J. Physiol. 500 (1997) 319-329
46. Hoyle G.W., Graham R.M., Finkelstein J.B., Nguyen K.P., Gozal D., and Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am. J. Respir. Cell Mol. Biol. 18 (1998) 149-157
47. Hunter D.D., Myers A.C., and Undem B.J. Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons. Am. J. Respir. Crit. Care Med. 161 (2000) 1985-1990
48. Ind P.W., Dixon C.M., Fuller R.W., and Barnes P.J. Anticholinergic blockade of beta-blocker-induced bronchoconstriction. Am. Rev. Respir. Dis. 139 (1989) 1390-1394
49. Jammes Y., Fornaris E., Mei N., and Barrat E. Afferent and efferent components of the bronchial vagal branches in cats. J. Auton. Nerv. Syst. 5 (1982) 165-176
50. Jammes Y., and Mei N. Assessment of the pulmonary origin of bronchoconstrictor vagal tone. J. Physiol. 291 305-316 (1979) 305-316
51. Jensen D., Amjadi K., Harris-McAllister V., Webb K.A., and O'Donnell D.E. Mechanisms of dyspnoea relief and improved exercise endurance after furosemide inhalation in COPD. Thorax 63 (2008) 606-613
52. Joad J.P., Kott K.S., and Bonham A.C. Nitric oxide contributes to substance P-induced increases in lung rapidly adapting receptor activity in guinea-pigs. J. Physiol. 503 (1997) 635-643
53. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Hogestatt E.D., Meng I.D., and Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
54. Kajekar R., Proud D., Myers A.C., Meeker S.N., and Undem B.J. Characterization of vagal afferent subtypes stimulated by bradykinin in guinea pig trachea. J. Pharmacol. Exp. Ther. 289 (1999) 682-687
55. Kassel O., de Blay F., Duvernelle C., Olgart C., Israel-Biet D., Krieger P., Moreau L., Muller C., Pauli G., and Frossard N. Local increase in the number of mast cells and expression of nerve growth factor in the bronchus of asthmatic patients after repeated inhalation of allergen at low-dose. Clin. Exp. Allergy 31 (2001) 1432-1440
56. Kaufman M.P., Coleridge H.M., Coleridge J.C., and Baker D.G. Bradykinin stimulates afferent vagal C-fibers in intrapulmonary airways of dogs. J. Appl. Physiol. 48 (1980) 511-517
57. Kay I.S., and Armstrong D.J. MDL 72222 (a selective 5-HT3 receptor antagonist) prevents stimulation of intrapulmonary C fibres by pulmonary embolization in anaesthetized rabbits. Exp. Physiol. 76 (1991) 213-218
58. Keh S.M., Facer P., Simpson K.D., Sandhu G., Saleh H.A., and Anand P. Increased nerve fiber expression of sensory sodium channels Nav1.7, Nav1.8, and Nav1.9 in rhinitis. Laryngoscope 118 (2008) 573-579
59. Kesler B.S., and Canning B.J. Regulation of baseline cholinergic tone in guinea-pig airway smooth muscle. J. Physiol. 518 (1999) 843-855
60. Kollarik M., and Undem B.J. Mechanisms of acid-induced activation of airway afferent nerve fibres in guinea-pig. J. Physiol. 543 (2002) 591-600
61. Kollarik M., and Undem B.J. Activation of bronchopulmonary vagal afferent nerves with bradykinin, acid and vanilloid receptor agonists in wild-type and TRPV1-/- mice. J. Physiol. 555 (2004) 115-123
62. Kummer W., Fischer A., Kurkowski R., and Heym C. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 49 (1992) 715-737
63. Kwong K., Carr M.J., Gibbard A., Savage T.J., Singh K., Jing J., Meeker S., and Undem B.J. Voltage-gated sodium channels in nociceptive versus non-nociceptive nodose vagal sensory neurons innervating guinea pig lungs. J. Physiol. 586 (2008) 1321-1336
64. Lankiewicz S., Lobitz N., Wetzel C.H., Rupprecht R., Gisselmann G., and Hatt H. Molecular cloning, functional expression, and pharmacological characterization of 5-hydroxytryptamine3 receptor cDNA and its splice variants from guinea pig. Mol. Pharmacol. 53 (1998) 202-212
65. Lee L.Y. Respiratory sensations evoked by activation of bronchopulmonary C-fibers. Respir. Physiol. Neurobiol. 167 (2009) 26-35
66. Lee L.Y., Burki N.K., Gerhardstein D.C., Gu Q., Kou Y.R., and Xu J. Airway irritation and cough evoked by inhaled cigarette smoke: role of neuronal nicotinic acetylcholine receptors. Pulm. Pharmacol. Ther. 20 (2007) 355-364
67. Lee L.Y., Gerhardstein D.C., Wang A.L., and Burki N.K. Nicotine is responsible for airway irritation evoked by cigarette smoke inhalation in men. J. Appl. Physiol. 75 (1993) 1955-1961
68. Lee M.G., Kollarik M., Chuaychoo B., and Undem B.J. Ionotropic and metabotropic receptor mediated airway sensory nerve activation. Pulm. Pharmacol. Ther. 17 (2004) 355-360
69. 2 on vagal bronchopulmonary C-fiber afferents during airway inflammation. J. Appl. Physiol. 99 (2005) 1704-1711
70. Lindsay R.M., and Harmar A.J. Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337 (1989) 362-364
71. Lundberg L.E., Jorum E., Holm E., and Torebjork H.E. Intra-neural electrical stimulation of cutaneous nociceptive fibres in humans: effects of different pulse patterns on magnitude of pain. Acta Physiol. Scand. 146 (1992) 41-48
72. Malin S.A., Molliver D.C., Koerber H.R., Cornuet P., Frye R., Albers K.M., and Davis B.M. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J. Neurosci. 26 (2006) 8588-8599
73. Mamet J., Baron A., Lazdunski M., and Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 22 (2002) 10662-10670
74. Mao D., Yasuda R.P., Fan H., Wolfe B.B., and Kellar K.J. Heterogeneity of nicotinic cholinergic receptors in rat superior cervical and nodose Ganglia. Mol. Pharmacol. 70 (2006) 1693-1699
75. Marantz M.J., Vincent S.G., and Fisher J.T. Role of vagal C-fiber afferents in the bronchomotor response to lactic acid in the newborn dog. J. Appl. Physiol. 90 (2001) 2311-2318
76. Marks G.B., Yates D.H., Sist M., Ceyhan B., De Campos M., Scott D.M., and Barnes P.J. Respiratory sensation during bronchial challenge testing with methacholine, sodium metabisulphite, and adenosine monophosphate. Thorax 51 (1996) 793-798
77. Mazzone S.B., and Canning B.J. Central nervous system control of the airways: pharmacological implications. Curr. Opin. Pharmacol. 2 (2002) 220-228
78. - channels regulate citric acid cough in guinea pigs. J. Appl. Physiol. 101 (2006) 635-643
79. Mazzone S.B., Mori N., and Canning B.J. Synergistic interactions between airway afferent nerve subtypes regulating the cough reflex in guinea-pigs. J. Physiol. 569 (2005) 559-573
80. McIlwrath S.L., Hu J., Anirudhan G., Shin J.B., and Lewin G.R. The sensory mechanotransduction ion channel ASIC2 (acid sensitive ion channel 2) is regulated by neurotrophin availability. Neuroscience 131 (2005) 499-511
81. Moosavi S.H., Binks A.P., Lansing R.W., Topulos G.P., Banzett R.B., and Schwartzstein R.M. Effect of inhaled furosemide on air hunger induced in healthy humans. Respir. Physiol. Neurobiol. 156 (2007) 1-8
82. Nassenstein C., Dawbarn D., Pollock K., Allen S.J., Erpenbeck V.J., Spies E., Krug N., and Braun A. Pulmonary distribution, regulation, and functional role of Trk receptors in a murine model of asthma. J. Allergy Clin. Immunol. 118 (2006) 597-605
83. Nassenstein C., Kammertoens T., Veres T.Z., Uckert W., Spies E., Fuchs B., Krug N., and Braun A. Neuroimmune crosstalk in asthma: dual role of the neurotrophin receptor p75NTR. J. Allergy Clin. Immunol. 120 (2007) 1089-1096
84. Nassenstein C., Kwong K., Taylor-Clark T., Kollarik M., Macglashan D.M., Braun A., and Undem B.J. Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J. Physiol. 586 (2008) 1595-1604
85. Nishino T., Ide T., Sudo T., and Sato J. Inhaled furosemide greatly alleviates the sensation of experimentally induced dyspnea. Am. J. Respir. Crit. Care Med. 161 (2000) 1963-1967
86. Path G., Braun A., Meents N., Kerzel S., Quarcoo D., Raap U., Hoyle G.W., Nockher W.A., and Renz H. Augmentation of allergic early-phase reaction by nerve growth factor. Am. J. Respir. Crit. Care Med. 166 (2002) 818-826
87. Pelleg A., and Hurt C.M. Mechanism of action of ATP on canine pulmonary vagal C fibre nerve terminals. J. Physiol. 490 (1996) 265-275
88. Richardson C.A., Herbert D.A., and Mitchell R.A. Modulation of pulmonary stretch receptors and airway resistance by parasympathetic efferents. J. Appl. Physiol. 57 (1984) 1842-1849
89. Riedel F., Oberdieck B., Streckert H.J., Philippou S., Krusat T., and Marek W. Persistence of airway hyperresponsiveness and viral antigen following respiratory syncytial virus bronchiolitis in young guinea-pigs. Eur. Respir. J. 10 (1997) 639-645
90. Sarkar S., Hobson A.R., Furlong P.L., Woolf C.J., Thompson D.G., and Aziz Q. Central neural mechanisms mediating human visceral hypersensitivity. Am. J. Physiol. Gastrointest. Liver Physiol. 281 (2001) G1196-G1202
91. Saroea H.G., Inman M.D., and O'Byrne P.M. U46619-induced bronchoconstriction in asthmatic subjects is mediated by acetylcholine release. Am. J. Respir. Crit. Care Med. 151 (1995) 321-324
92. Schmelz M., Schmidt R., Weidner C., Hilliges M., Torebjork H.E., and Handwerker H.O. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J. Neurophysiol. 89 (2003) 2441-2448
93. Sheppard D., Epstein J., Skoogh B.E., Bethel R.A., Nadel J.A., and Boushey H.A. Variable inhibition of histamine-induced bronchoconstriction by atropine in subjects with asthma. J. Allergy Clin. Immunol. 73 (1984) 82-87
94. Shin J., Cho H., Hwang S.W., Jung J., Shin C.Y., Lee S.Y., Kim S.H., Lee M.G., Choi Y.H., Kim J., Haber N.A., Reichling D.B., Khasar S., Levine J.D., and Oh U. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 10150-10155
95. Shu X., and Mendell L.M. Acute sensitization by NGF of the response of small-diameter sensory neurons to capsaicin. J. Neurophysiol. 86 (2001) 2931-2938
96. Simone P., Robuschi M., Vaghi A., Fasano W., and Bianco S. Prevention of fog-induced bronchospasm by high doses of ipratropium bromide in asthmatics. Respiration 50 (1986) 209-211
97. Skloot G., Permutt S., and Togias A. Airway hyperresponsiveness in asthma: a problem of limited smooth muscle relaxation with inspiration. J. Clin. Invest. 96 (1995) 2393-2403
98. Springall D.R., Cadieux A., Oliveira H., Su H., Royston D., and Polak J.M. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J. Auton. Nerv. Syst. 20 (1987) 155-166
99. Stein A.T., Ufret-Vincenty C.A., Hua L., Santana L.F., and Gordon S.E. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J. Gen. Physiol. 128 (2006) 509-522
100. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., McIntyre P., Jegla T., Bevan S., and Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
101. Sudo T., Hayashi F., and Nishino T. Responses of tracheobronchial receptors to inhaled furosemide in anesthetized rats. Am. J. Respir. Crit. Care Med. 162 (2000) 971-975
102. Szallasi A., Cortright D.N., Blum C.A., and Eid S.R. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat. Rev. Drug Discov. 6 (2007) 357-372
103. Taguchi O., Kikuchi Y., Hida W., Iwase N., Okabe S., Chonan T., and Takishima T. Prostaglandin E2 inhalation increases the sensation of dyspnea during exercise. Am. Rev. Respir. Dis. 145 (1992) 1346-1349
104. Taguchi O., Kikuchi Y., Hida W., Iwase N., Satoh M., Chonan T., and Takishima T. Effects of bronchoconstriction and external resistive loading on the sensation of dyspnea. J. Appl. Physiol. 71 (1991) 2183-2190
105. Taylor-Clark T., and Undem B.J. Transduction mechanisms in airway sensory nerves. J. Appl. Physiol. 101 (2006) 950-959
106. Taylor-Clark T.E., Kollarik M., Macglashan D.W., and Undem Jr. B.J. Nasal sensory nerve populations responding to histamine and capsaicin. J. Allergy Clin. Immunol. 116 (2005) 1282-1288
107. Taylor-Clark T.E., Undem B.J., Macglashan Jr. D.W., Ghatta S., Carr M.J., and McAlexander M.A. Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1). Mol. Pharmacol. 73 (2008) 274-281
108. Taylor-Clark T.E., McAlexander M.A., Nassenstein C., Sheardown S.A., Wilson S., Thornton J., Carr M.J., and Undem B.J. Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal. J. Physiol. 15 (2008) 3447-3459
109. Tetzlaff K., Leplow B., ten Thoren C., and Dahme B. Perception of dyspnea during histamine- and methacholine-induced bronchoconstriction. Respiration 66 (1999) 427-433
110. Tokime K., Katoh-Semba R., Yamanaka K., Mizoguchi A., and Mizutani H. Enhanced production and secretion of glial cell line-derived neurotrophic factor and nerve growth factor from the skin in atopic dermatitis mouse model. Arch. Dermatol. Res. 300 (2008) 343-352
111. Tollet J., Everett A.W., and Sparrow M.P. Development of neural tissue and airway smooth muscle in fetal mouse lung explants: a role for glial-derived neurotrophic factor in lung innervation. Am. J. Respir. Cell Mol. Biol. 26 (2002) 420-429
112. Treede R.D., Meyer R.A., Raja S.N., and Campbell J.N. Peripheral and central mechanisms of cutaneous hyperalgesia. Prog. Neurobiol. 38 (1992) 397-421
113. Trevisani M., Siemens J., Materazzi S., Bautista D.M., Nassini R., Campi B., Imamachi N., Andre E., Patacchini R., Cottrell G.S., Gatti R., Basbaum A.I., Bunnett N.W., Julius D., and Geppetti P. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 13519-13524
114. Undem B.J., Chuaychoo B., Lee M.G., Weinreich D., Myers A.C., and Kollarik M. Subtypes of vagal afferent C-fibres in guinea-pig lungs. J. Physiol. 556 (2004) 905-917
115. Virchow J.C., Julius P., Lommatzsch M., Luttmann W., Renz H., and Braun A. Neurotrophins are increased in bronchoalveolar lavage fluid after segmental allergen provocation. Am. J. Respir. Crit. Care Med. 158 (1998) 2002-2005
116. Wagner E.M., and Jacoby D.B. Methacholine causes reflex bronchoconstriction. J. Appl. Physiol. 86 (1999) 294-297
117. Widdicombe J. Reflexes from the lungs and airways: historical perspective. J. Appl. Physiol. 101 (2006) 628-634
118. Widdicombe J. Lung afferent activity: implications for respiratory sensation. Respir. Physiol. Neurobiol. 167 (2009) 2-8
119. Wilson N., Dixon C., and Silverman M. Bronchial responsiveness to hyperventilation in children with asthma: inhibition by ipratropium bromide. Thorax 39 (1984) 588-593
120. Woolf C.J. Evidence for a central component of post-injury pain hypersensitivity. Nature 306 (1983) 686-688
121. Woolf C.J. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106 (2007) 864-867
122. Xu J., Yang W., Zhang G., Gu Q., and Lee L.Y. Calcium transient evoked by nicotine in isolated rat vagal pulmonary sensory neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 292 (2007) L54-L61
123. Xue Q., Jong B., Chen T., and Schumacher M.A. Transcription of rat TRPV1 utilizes a dual promoter system that is positively regulated by nerve growth factor. J. Neurochem. 101 (2007) 212-222